Gains in Grain Yield: A Pair of Spikelets Makes All the Difference, Even When One Is Sterile

Mother Nature has a way of keeping seemingly useless structures around millions of years. Such structures are likely to have a use that is not obvious, although they could also be remnants of the evolutionary past without extant function or nonfunctional but harmless byproducts of a different adaptive feature. In a fascinating study, Taylor AuBuchon-Elder and colleagues (AuBuchon-Elder et al., 2020) report on the sterile spiklelet of sorghum (Sorghum bicolor) and related grasses and provide support for the idea that this curious structure has been maintained for over 15 million years because it serves an important function.

Sorghum belongs to the grass tribe Andropogoneae, where paired spikelets house florets (Kellogg, 2015). In sorghum, a sterile (non-seed-bearing) short-stalked pedicellate spikelet (PS) pairs with a fertile, stalkless sessile spikelet (SS) that ultimately bears grain. Additionally, the SS is awned. In wheat, awns can assimilate and transfer carbon to grain (Grundbacher, 1963). PS or awn function in sorghum has not been reported. With these observations and unknowns, the authors set out to understand the significance of the PS and awns in sorghum and related grasses.

Could the PS, awn, or both be a source of photosynthate for the SS? To find out, the authors initially conducted a series of ¹⁴C labeling and pulse-chase experiments. For ¹⁴C labeling, PS had significantly more ¹⁴CO₂ uptake compared to SS or awns. Additionally, a 24-h pulse-chase experiment in intact panicles showed a decrease in percent ¹⁴C in PS and concomitant percent increase in SS. This observation indicated that the ¹⁴C had translocated from PS to SS. The idea that PS could be a carbon source made sense because the authors observed stomata on the surface of PS, but not on SS or awns. Stomata are epidermal pores where CO₂ enters the organ for photosynthesis. The authors found ¹⁴C labeling and pulse-chase results, along with appearance of stomata, to be consistent in two species distantly related to sorghum, Themeda triandra and Andropogon schirensis, which nicely broadened the context of their findings.

If the PS is a carbon source, metabolites produced by photosynthesis should be detectable. The authors explored this hypothesis in intact panicles of sorghum and T. triandra with time course exposure to ¹³CO₂ followed by liquid chromatography-tandem mass spectrometry. The authors cast a wide net in seining for metabolites from C₄, C₃, Suc, or starch pathways. Consistent with previous ¹⁴C labeling, PS had more ¹³C than SS or awns. Time course labeling showed the percent of unlabeled isotopologue fractions for individual metabolites of photosynthesis decreased at the early stages of ¹³CO₂ feeding, indicating carbon assimilation. Similarly, metabolites showed ¹³C enrichment within 5 min of labeling. The authors conducted transcriptomic analysis of leaf, PS, SS, and awns from the two species and filtered the data for differentially expressed genes encoding central carbon metabolic enzymes. In support, they found PS accumulated transcripts related to photosynthesis; likewise, these genes were downregulated in awns and SS.

PS have features of a carbon source; SS and awns have sink-like characteristics. How might this relationship impact yield? To address this question, the authors utilized four genotypes with diverse spikelet morphology and simply either detached the PS or left it intact on panicles at anthesis. When the panicles reached maturity, seed weights were collected. Importantly, the authors found a significant ∼8.8% reduction in yield between controls (intact) and treatment (detached) across all genotypes (see figure). Across individual genotypes, mean seed weights dropped from 8 to 13%, also suggesting that genetic variation in this trait might be leveraged to improve yield.

Detachment of the Sterile Pedicellate Spikelet Reduces Yield and Fitness.

Removal of the sterile PS reduces grain weight in the fertile SS, represented in box and whisker plots as combined average weight for four sorghum genotypes.

(Adapted from AuBuchon-Elder et al. [2020], Figure 7.)

Photosynthetic PS in the Andropogoneae, albeit reduced in size, have not gone unnoticed by Mother Nature. Rather, they are significant structures that increase yield in domesticated sorghum and fitness in its wild relatives. AuBuchon-Elder et al. (2020) have provided a solid foundation for future opportunities to improve sorghum. With a reference genome sequence (Paterson et al., 2009) and being amenable to genome engineering through transformation (Sander, 2019), prospects for gains in sorghum yield are far from sterile.